Abstract
Escherichia coli cells are capable of complex regulatory responses to environmental conditions and stresses. In some circumstances, the response includes an increase in the mutation rate, effectively mutagenizing the genome. The classic example is the SOS response to DNA damage. Recent work indicates that other environmental stresses can also result in mutation of the genome. Modulation of mutation rate may be a more prevalent stress response than previously thought. In this review we focus on genome-wide mutation inE. coli cells subjected to a nonlethal genetic selection for reversion of alac frameshift allele. Reversion of thelac frameshift allele occurs via a novel mechanism that requires homologous recombination functions, and is enhanced by transiently diminished postsynthesis mismatch repair. A model for recombination-dependent stationary-phase mutation will be presented and its relevance for genome-wide mutation discussed.
Similar content being viewed by others
References
Andersson D. I., Slechta E. S. and Roth J. R. 1998 Evidence that gene amplification underlies adaptive mutability of the bacteriallac operon.Science 282, 1133–1135.
Asai T., Bates D. B. and Kogoma T. 1994 DNA replication triggered by double-stranded breaks inE. coli: dependence on homologous recombination functions.Cell 78, 1051–1061.
Brégeon D., Matic I., Radman M. and Taddei F. 1999 Inefficient mismatch repair: genetic defects and down regulation.J. Genet. 78, 21–28 (this issue).
Bridges B. A. 1997 Hypermutation under stress.Nature 387, 557–558.
Cairns J. and Foster P. L. 1991 Adaptive reversion of a frameshift mutation inEscherichia coli.Genetics 128, 695–701.
Demerec M. 1962 “Selfers” attributed to unequal crossovers inSalmonella.Proc Natl. Acad. Sci. USA 48, 1695–1704.
Demerec M. 1963 Selfer mutants ofSalmonella typhimurium.Genetics 48, 1519–1531.
Esposito M. S. and Bruschi C. V. 1993 Diploid yeast cells yield homozygous spontaneous mutations.Curr. Genet. 23, 430–434.
Foster P. L. 1993 Adaptive mutation: the uses of adversity.Annu. Rev. Microbiol. 47, 467–504.
Foster P. L. 1997 Nonadaptive mutations occur in the F′ episome during adaptive mutation conditions inEscherichia coli.J. Bacteriol. 179, 1550–1554.
Foster P. L. and Trimarchi J. M. 1994 Adaptive reversion of a frameshift mutation inEscherichia coli by simple base deletions in homopolymeric runs.Science 265, 407–409.
Foster P. L. and Trimarchi J. M. 1995a Adaptive reversion of an episomal frameshift mutation inEscherichia coli requires conjugal functions but not actual conjugation.Proc. Natl. Acad. Sci. USA 92, 5487–5490.
Foster P. L. and Trimarchi J. M. 1995b Conjugation is not required for adaptive reversion of an episomal frameshift mutation inEscherichia coli.J. Bacteriol. 177, 6670–6671.
Foster P. L., Gudmundsson G., Trimarchi J. M., Cai H. and Goodman M. F. 1995 Proofreading-defective DNA polymerase II increases adaptive mutation inEscherichia coli.Proc. Natl. Acad. Sci. USA 92, 7951–7955.
Foster P. L., Trimarchi J. M. and Maurer R. A. 1996 Two enzymes, both of which process recombination intermediates, have opposite effects on adaptive mutation inEscherichia coli.Genetics 142, 25–37.
Galitski T. and Roth J. R. 1995 Evidence that F′ transfer replication underlies apparent adaptive mutation.Science 268, 421–423.
Harris R. S. 1997 On a molecular mechanism of adaptive mutation. Ph.D. thesis, University of Alberta, Edmonton, Canada.
Harris R. S., Longerich S. and Rosenberg S. M. 1994 Recombination in adaptive mutation.Science 264, 258–260.
Harris R. S., Ross K. J. and Rosenberg S. M. 1996 Opposing roles of the Holliday junction processing systems ofEscherichia coli in recombination-dependent adaptive mutation.Genetics 142, 681–691.
Harris R. S., Bull H. J. and Rosenberg S. M. 1997a A direct role for DNA polymerase III in adaptive reversion of a frameshift mutation inEscherichia coli.Mutat. Res. 375, 19–24.
Harris R. S., Feng G., Ross K. J., Sidhu R., Thulin C., Longerich S., Szigety S. K., Winkler M. E. and Rosenberg S. M. 1997b Mismatch repair protein MutL becomes limiting during stationary-phase mutation.Genes Dev. 11, 2426–2437.
Harris R. S., Feng G., Ross K. J., Sidhu R., Thulin C., Longerich S., Szigety S. K., Hastings P. J., Winkler M. E. and Rosenberg S. M. 1999a Mismatch repair is diminished during stationary-phase mutation.Rev. Mutat. Res. 434 (in press).
Harris R. S., Kong Q. and Maizels N. 1999b Somatic hypermutation and the three R’s: repair, replication and recombination.Mutat. Res. 436, 157–178.
Hastings P. J. and Rosenberg S. M. 1992 Gene conversion. InEncyclopedia of immunology (ed. I. M. Roittet al.), pp. 602–605. Academic Press, New York.
Hengge-Aronis R. 1996 Regulation of gene expression during entry into stationary phase. InEscherichia coli and Salmonella: cellular and molecular biology (ed. F. C. Neidhardtet al.), pp. 1497–1512. ASM Press, Washington, DC.
Holbeck S. L. and Strathern J. N. 1997 A role for REV3 in mutagenesis during double-strand break repair inSaccharomyces cerevisiae.Genetics 147, 1017–1024.
Kreuzer K. M. and Morrical S. W. 1994 Initiation of DNA replication. InMolecular biology of bacteriophage T4 (ed. J. Karam), pp. 28–42. ASM Press, Washington, DC.
Kuzminov A. 1995 Collapse and repair of replication forks inEscherichia coli.Mol. Microbiol. 16, 373–384.
Kuzminov A. and Stahl F. W. 1999 Double-strand end repair via the RecBC pathway inEscherichia coli primes DNA replication.Genes Dev. 13, 345–356.
Lloyd R. G. 1991 Conjugational recombination in resolvase-deficientruvC mutants ofEscherichia coli depends onrecG.J. Bacteriol. 173, 5414–5418.
Lloyd R. G. and Low K. B. 1996 Homologous recombination. InEscherichia coli and Salmonella: cellular and molecular biology (ed. F. C. Neidhardtet al.), pp. 2236–2255. ASM Press, Washington, DC.
Lombardo M.-J., Harris R. S. and Rosenberg S. M. 1998 Stressful lifestyle associated mutation in microorganisms. InPlant responses to environmental stresses: from phytohormones to genome reorganization (ed. H. R. Lerner). Marcel Dekker, New York (in press).
Lombardo M.-J., Torkelson J., Bull H. J., McKenzie G. J. and Rosenberg S. M. 1999 Mechanisms of genome-wide hypermutation in stationary phase.Ann. N. Y. Acad. Sci. 870, 275–289.
Longerich S., Galloway A. M., Harris R. S., Wong C. and Rosenberg S. M. 1995 Adaptive mutation sequences reproduced by mismatch repair deficiency.Proc. Natl. Acad. Sci. USA 92, 12017–12020.
McKenzie G. J., Lombardo M.-J. and Rosenberg S. M. 1998 Recombination-dependent mutation inEscherichia coli occurs in stationary phase.Genetics 149, 1163–1165.
Magni G. E. 1963 The origin of spontaneous mutation during meiosis.Proc. Natl. Acad. Sci. USA 50, 975–980.
Magni G. E. and von Borstel R. C. 1962 Different rates of spontaneous mutation during mitosis and meiosis in yeast.Genetics 47, 1097–1108.
Michel B., Ehrlich S. D. and Uzest M. 1997 DNA double-strand breaks caused by replication arrest.EMBO J. 16, 430–438.
Miesel L. and Roth J. R. 1996 Evidence that functions of the “RecF pathway” contribute to RecBCD-dependent transductional recombination.J. Bacteriol. 178, 3146–3155.
Modrich P. 1995 Mismatch repair, genetic stability and tumour avoidance.Philos. Trans. R. Soc. London B347, 89–95.
Mosig G. 1994 Homologous recombination. InMolecular biology of bacteriophage T4 (ed. J. Karam), pp. 54–82. ASM Press, Washington, DC.
Myers R. S. and Stahl F. W. 1994χ and RecBCD enzyme ofEscherichia coli.Annu. Rev. Genet. 28, 49–70.
Paszewski A. and Surzycki S. 1964 “Selfers” and high mutation rate during meiosis inAscobolus immersus.Nature 204, 809.
Radicella J. P., Park P. U. and Fox M. S. 1995 Adaptive mutation inEscherichia coli: a role for conjugation.Science 268, 418–420.
Razavy H., Szigety S. K. and Rosenberg S. M. 1996 Evidence for both 3′ and 5′ single-strand DNA ends in intermediates in Chi stimulated recombinationin vivo.Genetics 142, 333–339.
Roca A. I. and Cox M. M. 1997 RecA protein: structure, function, and role in recombinational DNA repair.Prog. Nucl. Acid Res. Mol. Biol. 56, 129–223.
Rosenberg S. M. 1994 In pursuit of a molecular mechanism for adaptive mutation.Genome 37, 893–899.
Rosenberg S. M. 1997 Mutation for survival.Curr. Opin. Genet. Dev. 7, 829–834.
Rosenberg S. M. and Hastings P. J. 1991 The split-end model for homologous recombination at double-strand breaks and at Chi.Biochimie 73, 385–397.
Rosenberg S. M. and Motamedi M. R. 1999 Homologous recombination during bacterial conjugation. InEncyclopedia of life sciences. MacMillan Reference, London (in press).
Rosenberg S. M., Longerich S., Gee P. and Harris R. S. 1994 Adaptive mutation by deletions in small mononucleotide repeats.Science 265, 405–407.
Rosenberg S. M., Harris R. S. and Torkelson J. 1995 Molecular handles on adaptive mutation.Mol. Microbiol. 18, 185–189.
Rosenberg S. M., Harris R. S., Longerich S. and Galloway A. M. 1996 Recombination-dependent mutation in non-dividing cells.Mutat. Res. 350, 69–76.
Rosenberg S. M., Thulin C. and Harris R. S. 1998 Transient and heritable mutators in adaptive evolution in the lab and in nature.Genetics 148, 1559–1566.
Skalka A. 1974 A replicator’s view of recombination (and repair). InMechanisms of recombination (ed. G. Grell), pp. 421–431. Plenum, New York.
Smith B. T. and Walker G. C. 1998 Mutagenesis and more:umuDC and theEscherichia coli SOS response.Genetics 148, 1599–1610.
Stahl F. W. 1988 A unicorn in the garden.Nature 335, 112–113.
Strathern J. N., Shafer B. K. and McGill C. B. 1995 DNA synthesis errors associated with double-strand-break repair.Genetics 140, 965–972.
Taddei F., Matic I. and Radman M. 1995 cAMP-dependent SOS induction and mutagenesis in resting bacterial populations.Proc. Natl. Acad. Sci. USA 92, 11736–11740.
Taddei F., Halliday J. A., Matic I. and Radman M. 1997 Genetic analysis of mutagenesis in agingEscherichia coli colonies.Mol. Gen. Genet. 256, 277–281.
Tlsty T. D., Albertini A. M. and Miller J. H. 1984 Gene amplification in thelac region ofE. coli.Cell 37, 217–224.
Torkelson J., Harris R. S., Lombardo M.-J., Nagendran J., Thulin C. and Rosenberg S. M. 1997 Genome-wide hypermutation in a subpopulation of stationary-phase cells underlies recombination-dependent adaptive mutation.EMBO J. 16, 3303–3311.
Walker G. C. 1996 The SOS response ofEscherichia coli. InEscherichia coli and Salmonella: cellular and molecular biology (ed. F. C. Neidhardtet al.), pp. 1400–1416. ASM Press, Washington, DC.
Walker G. C. 1998 Skiing the black diamond slope: progress on the biochemistry of translesion DNA synthesis.Proc. Natl. Acad. Sci. USA 95, 10348–10350.
Zambrano M. M. and Kolter R. 1996 GASPing for life in stationary phase.Cell 86, 181–184.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Lombardo, MJ., Rosenberg, S.M. Hypermutation in stationary-phaseE. coli: tales from thelac operon. J Genet 78, 13–20 (1999). https://doi.org/10.1007/BF02994698
Issue Date:
DOI: https://doi.org/10.1007/BF02994698